Serological Profile of Foot-And-Mouth Disease in Wildlife Populations Of
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Nardo et al. Veterinary Research (2015) 46:77 DOI 10.1186/s13567-015-0213-0 VETERINARY RESEARCH RESEARCH ARTICLE Open Access Serological profile of foot-and-mouth disease in wildlife populations of West and Central Africa with special reference to Syncerus caffer subspecies Antonello Di Nardo1,2*, Geneviève Libeau3, Bertrand Chardonnet4, Philippe Chardonnet5, Richard A Kock6, Krupali Parekh2, Pip Hamblin2, Yanmin Li2,8, Satya Parida2 and Keith J Sumption7 Abstract The role which West and Central African wildlife populations might play in the transmission dynamics of FMD is not known nor have studies been performed in order to assess the distribution and prevalence of FMD in wild animal species inhabiting those specific regions of Africa. This study reports the FMD serological profile extracted from samples (n =696) collected from wildlife of West and Central Africa between 1999 and 2003. An overall prevalence of FMDV NSP reactive sera of 31.0% (216/696) was estimated, where a significant difference in seropositivity (p = 0.000) was reported for buffalo (64.8%) as opposed to other wild animal species tested (17.8%). Different levels of exposure to the FMDV resulted for each of the buffalo subspecies sampled (p = 0.031): 68.4%, 50.0% and 0% for Nile Buffalo, West African Buffalo and African Forest Buffalo, respectively. The characterisation of the FMDV serotypes tested for buffalo found presence of antibodies against all the six FMDV serotypes tested, although high estimates for type O and SAT 3 were reported for Central Africa. Different patterns of reaction to the six FMDV serotypes tested were recorded, from sera only positive for a single serotype to multiple reactivities. The results confirmed that FMDV circulates in wild ruminants populating both West and Central Africa rangelands and in particular in buffalo, also suggesting that multiple FMDV serotypes might be involved with type O, SAT 2 and SAT 1 being dominant. Differences in serotype and spill-over risk between wildlife and livestock likely reflect regional geography, historical circulation and differing trade and livestock systems. Introduction from a completely inapparent to a rare acutely lethal in- Foot-and-mouth disease (FMD) is an economically dev- fection, making the diagnosis difficult either because the astating disease of intensive livestock farming and high variability in the severity of presenting clinical signs is production animals, caused by a virus member of the greater than in domestic livestock or because it tends to Apthovirus genus within the Picornaviridae family, and be subclinical for the particular species/virus combin- characterised by an acute and highly contagious vesicu- ation [2,3]. The transmission dynamic of FMD in sub- lar disease which can develop into persistent infection. Saharan Africa is mainly driven by two epidemiological Vesicular lesions resulting from FMD infection are cycles: one in which wildlife plays a significant role in mainly found in tongue, lips and feet but in some cases maintaining and spreading the disease to other suscep- lesions also can occur in snout, muzzle, teats, skin and tible wild and/or domestic ruminants [4-6], whilst with rumen. The disease is characterised by a very short incu- the second the virus is solely transmitted within domes- bation period and high level of virus excretion, particu- tic populations and hence is independent of wildlife. larly in pigs [1]. In wildlife, the FMD pathogenesis varies More than 70 wild animal species have been demon- strated to be susceptible to the FMD virus (FMDV) ei- * Correspondence: [email protected] ther by natural infection or by experimental challenge, 1Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, and on several occasions the virus has been isolated United Kingdom from naturally infected animals [7]. Among these, Cape 2 The Pirbright Institute, Pirbright, Surrey, Woking, United Kingdom buffalo (Syncerus caffer caffer) has been clearly shown to Full list of author information is available at the end of the article © 2015 Nardo et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Nardo et al. Veterinary Research (2015) 46:77 Page 2 of 16 serve as long-term maintenance host (i.e. carrier) for the seven FMDV serotypes have been reconstructed from Southern African Territories (SAT) FMDV serotypes wildlife samples collected from national parks and faunal [8-10], and in populations of Cape buffalo the virus has reserves of West and Central Africa. The aims of this been estimated to persist for 24 years or longer [11]. In- study were: firstly, to produce an overall picture of the fection in buffalo is subclinical and normally occurs in FMD prevalence in wildlife and mainly in buffalo subspe- calves as soon as maternal antibodies wane at 2–6 cies of West and Central Africa, also characterising risk months of age. Acutely infected buffalo provide sources factors likely associated with the observed prevalence; sec- of infection for other ruminants, both domestic and ondly, to identify the FMDV serotypes potentially circulat- wild, directly or through other species which have ing in resident buffalo populations within the study area. contracted the infection from buffalo [5,6]. Although the In addition, potential limitations of diagnostic testing pro- implication of the buffalo carriers in the epidemiology of cedures used have been evaluated. FMD has not been fully clarified, they have so far been shown to transmit the disease while in that state Materials and methods [4,8,12]. Phylogenetic relationships between SAT types Study population FMDV strains isolated from cattle and those carried by The study was undertaken on serum samples collected from buffalo have been reconstructed from different area of wild ruminants and pigs species during the African Wildlife southern Africa, proving that contacts between livestock Veterinary Project [24], as part of the Pan-African Rinder- and buffalo regularly result in FMD outbreaks among pest Campaign (PARC) and the subsequent programme for cattle [13,14]. Furthermore, available evidence based on the Pan-African Control of Epizootics (PACE) implemented FMDV genome sequencing indicates that impala (Aepy- in 34 countries across the African continent between 1986 ceros melampus) populations of the Kruger National and 2007. Wildlife species and sampling sites were selected Park – South Africa, usually become infected with SAT at the time according to susceptibility to the Rinderpest viruses derived from buffalo [5]. On occasions SAT line- (RP) virus, population biology (i.e. richness, gregarious ages were demonstrated to have been transmitted first behaviour, and seasonal movements), interface between from buffalo to impala and then from impala to cattle livestock and wildlife, and their availability for veterin- [6,15]. Conceived as such, impala can provide a conduit ary interventions. Sampling was performed using purpos- of infection between buffalo and livestock, acting as an ive sampling by immobilisation, opportunistic sampling by important intermediate between domestic and wild ru- cropping and/or hunting and during field investigations of minants and as an amplifying host in the context of reported episodes of disease and mortality. From the whole FMD transmission dynamics [16]. Presence of antibodies collection stored at the Centre de Coopération Internation- against the FMDV in several wildlife species has been ale en Recherche Agronomique pour le Développement documented in studies conducted in different countries (CIRAD), Montpellier – France, 696 sera collected be- of the African continent, but mainly within its eastern tween 1999 and 2003 were selected as representative of and southern regions [16-18]. In addition, serological wildlife populations present in West and Central Africa screenings implemented in East African countries have (Table 1; Figure 1). In addition, further 19 samples col- indicated potential infections of Cape buffalo with A and lected from cattle within the transfrontier area of the O FMDV serotypes [19-23], although current data do Central African Republic and Chad were included for not support the primary role of buffalo and other wild comparative purpose. Extracted aliquots were sent to The animal species in the transmission of those FMDV sero- Pirbright Institute, Pirbright – United Kingdom (UK), for types generally occurring in domestic ruminants. This diagnostic testing. represents an important pattern of the FMD transmis- sion dynamics in large parts of sub-Saharan Africa that Testing methodology still remains to be explained. Much is already known The sample collection was initially screened for antibodies about the role that Cape buffalo plays in the FMD epi- against the highly conserved NSP of the FMDV using the demiology, largely from studies conducted in South and PrioCHECK® FMDV NS Enzyme-Linked Immunosorbent East Africa; conversely, knowledge on the relationship Assay (ELISA) test kit (Prionics AG, Switzerland), accord- between FMDV and wildlife and/or other